Age‐specific reproduction in female Steller sea lions in Southeast Alaska

Abstract Age‐, region‐, and year‐specific estimates of reproduction are needed for monitoring wildlife populations during periods of ecosystem change. Population dynamics of Steller sea lions (Eumetopias jubatus) in Southeast Alaska varied regionally (with high population growth and survival in the north vs. the south) and annually (with reduced adult female survival observed following a severe marine heatwave event), but reproductive performance is currently unknown. We used mark‐resighting data from 1006 Steller sea lion females marked as pups at ~3 weeks of age from 1994 to 1995 and from 2001 to 2005 and resighted from 2002 to 2019 (to a maximum age of 25) to examine age‐, region‐, and year‐specific reproduction. In the north versus the south, age of first reproduction was earlier (beginning at age 4 vs. age 5, respectively) but annual birth probabilities of parous females were reduced by 0.05. In an average year pre‐heatwave, the proportion of females with pup at the end of the pupping season peaked at ages 12–13 with ~0.60/0.65 (north/south) with pup, ~0.30/0.25 with juvenile, and ~0.10 (both regions) without a dependent. In both regions, reproductive senescence was gradual after age 12: ~0.40, 0.40, and 0.20 of females were in these reproductive states, respectively, by age 20. Correcting for neonatal mortality, true birth probabilities at peak ages were 0.66/0.72 (north/south). No cost of reproduction on female survival was detected, but pup production remained lower (−0.06) after the heatwave event, which if sustained could result in population decline in the south. Reduced pup production and greater retention of juveniles during periods of poor prey conditions may be an important strategy for Steller sea lions in Southeast Alaska, where fine‐tuning reproduction based on nutritional status may improve the lifetime probability of producing pups under good conditions in a variable and less productive environment.


| INTRODUC TI ON
Age-structured survival and reproduction determine both individual fitness (Bouwhuis et al., 2012) and changes in population abundance and are therefore key demographic processes for monitoring natural populations (Eberhardt, 1985).In large mammal species characterized by low mass-specific metabolic rates and intrinsic rates of increase (Hennemann, 1983), population change is most sensitive to changes in adult survival probabilities (Gaillard et al., 2000).However, changes in birth probabilities may drive population change during the initial phases of growth (Albon et al., 2000), in increasing populations (Coulson & Hudson, 2003) and when reproduction is more annually variable and environmentally sensitive than adult survival (Coulson et al., 2005;Manlik et al., 2016 and references therein).Therefore, monitoring reproduction is critical for large mammal species, including annual and age-specific variability (e.g., recruitment and senescence) and covariance between survival and reproduction, which may alter outcomes of population models (Colchero et al., 2019;Doak et al., 2005).
The Steller sea lion, Eumetopias jubatus, an eared seal species of the family Otariidae, is an important top predator in the North Pacific Ocean occurring from California around the Pacific Rim to Alaska, Russia and Japan (King, 1983).Population declines of up to 80% from the 1970s to 2003 (Fritz et al., 2016) resulted in the listing of the species throughout much of its' range under the U.S. Endangered Species Act.Recent estimates of age-specific survival probabilities (Altukhov et al., 2015;Fritz et al., 2014;Hastings et al., 2011;Maniscalco, 2014;Warlick et al., 2022;Wright et al., 2017) are useful for population viability models, but age-specific information on reproduction is sparse.Models have relied on reproductive rate estimates from the 1970s and 1980s which were based on pregnancy rates of cross-sectional samples (Pitcher & Calkins, 1981;Pitcher et al., 1998) that assumed no reproductive senescence (York, 1994).Reproductive senescence is expected in nearly all mammals (Comizzoli & Ottinger, 2021) but remains unstudied in Steller sea lions.Birth probabilities are best provided by direct observations of known individual females during the pupping season due to high rates of late-term abortions (Pitcher & Calkins, 1981); longitudinal sampling of marked known-aged females provides ideal information (Le Boeuf et al., 2019).However, robust estimates of age-specific reproduction are available for less than half of the 15 extant otariid species (Childerhouse et al., 2010;Dabin et al., 2004;Kalberer et al., 2018;Lunn et al., 1994;McKenzie et al., 2007;Melin et al., 2012).
In addition to age effects, regional and annual shifts in reproduction may indicate reproductive strategies females use to cope with environmental variation, a primary concern for Steller sea lion conservation (NMFS, 2008).Population dynamics vary regionally and annually for Steller sea lions in Southeast Alaska.Regional differences suggest a more productive environment and/or reduced density dependence in the north (rookeries White Sisters and Graves Rocks) versus the south (rookeries Hazy and Forrester Islands; Figure 1) with high population growth, smaller population size, more restricted animal movements, larger neonates and high

T A X O N O M Y C L A S S I F I C A T I O N
Population ecology F I G U R E 1 Map of Steller sea lion rookeries in the Gulf of Alaska.Four rookeries (red stars) where pups were marked in Southeast Alaska were: Forrester Islands (south region), Hazy Islands (south region), White Sisters (north region), and Graves Rocks (north region); no pups were marked at a fifth small rookery Biali Rocks.Boxed = 1: Inian Islands, 2: Sea Lion Rocks Puffin Bay, and 3: Wolf Rock.
juvenile survival in the north, compared to population stability, large population size, smaller neonates, lower juvenile survival, higher survival cost of weaning for juveniles, and more extensive animal movements in the south, where the population is considered near carrying capacity (Hastings et al., 2011(Hastings et al., , 2021;;Jemison et al., 2018;Mathews et al., 2011;Pitcher et al., 2007).Therefore, regional differences in reproductive output may indicate female response to variation in environmental productivity and/or local abundance.
Annual variation in population dynamics may also indicate sea lion response to abrupt environmental change: an abrupt decline of −0.05 to −0.23 in adult female Steller sea lion survival occurred in Southeast Alaska, in Prince William Sound and at Chiswell Island (Figure 1) during and following the severe North Pacific marine heatwave of 2014-2016 (PMH; (PMH;Hastings et al., 2023).The effects of the PMH on reproduction are of interest because widescale and persistent changes in the Gulf of Alaska food web during the PMH are well documented (Arimitsu et al., 2021;Suryan et al., 2021), and food intake relative to whole-body energy balance strongly determines reproductive success in female mammals (Bronson, 1985;Wade & Schneider, 1992), including Steller sea lions (Pitcher et al., 1998).Whether reproductive state contributed to the high female mortality observed during the PMH is also of interest.The important trade-off between female survival and fecundity (Stearns, 1989) has not yet been documented for Steller sea lions (Maniscalco et al., 2014).Both reduced (due to energy costs of raising young) and increased (due to higher survival and reproduction in higher quality individuals) female survival have been associated with offspring production in other otariids (Beauplet et al., 2006;Boyd et al., 1995).Marine heatwaves are predicted to increase in frequency and severity with ocean warming (Oliver et al., 2018), and therefore current vital rate information is particularly needed for models addressing the effects of climate change on Steller sea lions and other marine mammal populations (Albouy et al., 2020).
Estimating otariid reproductive rates with mark-recapture studies may be challenging due to the need to estimate both pup production and juvenile retention (multiple reproductive states) with imperfect state detection.Otariids produce a single pup at a time (twinning is rare) and lactation is energetically demanding: females must feed during lactation (for at least 9-12 months in all but two species) to sustain both their own and their offspring's growth and survival (Bonner, 1984) which also requires them to remain nearshore ~year-round (Costa & Valenzuela-Toro, 2021).In nearly half of otariid species, including Steller sea lions, females may retain dependent juveniles for >1 year in lieu of new pup production (Hastings et al., 2021).Multiple potential reproductive states complicate studies of reproduction and associated statistical models because demographic and observational processes are often state dependent.Often, the detection of reproductive state is imperfect because when females are observed, they are not always physically associated with their offspring, and some states may not be definitively observed (e.g., nonbreeder or weaned; Hastings et al., 2021;Johnson et al., 2016).For statistical models to accurately estimate reproduction, female resighting and state detection probabilities must also be estimated.Modeling only two states (with and without pup) will not yield accurate estimates of reproduction when behavior varies significantly for females with juveniles versus those without a dependent.
In this study, we used appropriate models to address these complexities for mark-resighting data from 1006 Steller sea lion females marked as pups at 3 weeks of age at their natal rookeries in the northern and southern regions of Southeast Alaska (from 1994 to 1995 and from 2001 to 2005) and resighted from 2002 to 2019 to a maximum age of 25 years.Here, we estimate age-specific reproductive performance, and regional and year variation in reproductive performance, with particular interest in effects of the PMH on reproductive output, including an evaluation of the cost of reproduction to female survival.
During each marking session, a workable area on the rookery was chosen, usually containing 75-200 pups.All pups in the area were carefully corralled, monitored, and sampled by a large field crew (Hastings et al., 2009).All pups >20 kg were marked to ensure a representative sample; pups <20 kg were not branded but received a dye mark on their fur and/or a flipper tag.By marking at the end of the pupping season, few pups (<5%) were of insufficient weight and were likely the latest-born pups.We assume this method of obtaining a marked sample of Steller sea lion pups yielded a representative sample.Methods of animal handling, marking, and observation were approved by the Alaska Department of Fish and Game (ADFG) Institutional Animal Care and Use Committee and under permits issued by the US National Marine Fisheries Service (NMFS) to the ADFG.Branding has been used extensively as a method for permanent marking of pinnipeds, and several studies have reported a lack of effect on survival or animal health using this method (Hastings et al., 2009;McMahon et al., 2006;Merrick et al., 1996).This method was particularly required for Steller sea lions in Alaska for which very high tag loss rates for animals marked as pups and poor visibility of tags leading to insufficient resighting rates precluded the collection of vital rate information (Hastings et al., 2017;Merrick et al., 1996).
Resighting surveys of marked animals occurred at all rookeries and major haulouts in Southeast Alaska during dedicated large-scale boat-based surveys and one field camp each summer from 2002 to 2019 (Hastings et al., 2011;Pendleton et al., 2006) Prebreeder and No-Dependent were unobservable (i.e., could not be determined based on observation).On each occasion, sightings of females were coded as "0" if not seen, "u" if seen but reproductive state was uncertain, "B" if seen as With-Pup, and "J" if seen as With-Juvenile.The state "Prebreeder" ("P") occurred once per capture history on the initial release only, which was at age 0 for the 2001-2005 cohorts (Appendix 1).As described earlier, the 116 females from the 1994 and 1995 cohorts were not necessarily Prebreeders when first observed, but their first nonzero record in their capture histories was coded as such, and these females were treated separately when estimating recruitment probabilities, which instead accounted for the transitioning of these females into the population of knowable state after 2004.Fewer females were observed definitively With-Juvenile than With-Pup (211 vs. 902 female*year sightings; Appendix 2).
Few Steller sea lion females (1.9%-3.7%)can have both a dependent juvenile and pup during the pupping season (aka "triad"), in which case most often the juvenile is favored over the new pup by the end of the pupping season (Hastings et al., 2021;Maniscalco & Parker, 2009).Of 211 females With-Juvenile*year, only four (1.9%) were also observed with a pup during the survey window, and for these four cases, the pup data were replaced with the juvenile sightings.
Using these capture histories, we fitted multivariate state Cormack-Jolly-Seber models that allowed imperfect state detection and that were formulated as a hidden Markov process, such that maximum likelihood could be used for parameter estimation (Johnson et al., 2016;Laake et al., 2014).We used the R package marked (model "mvmscjs"; Laake et al., 2013;R Core Team, 2022) to estimate parameters and select models based on AIC (Burnham & Anderson, 2002).The models included five parameter types, three of which were nuisance parameters (i.e., of no biological interest but necessary for appropriate modeling of the data).Pollock, 1982).After 2004, survival probabilities and reproductive state transitions were estimated for the intervals between the fourth (i.e., last) occasion in a year to the first occasion of the next year.Survival was fixed to 1 and reproductive state transitions to 0 between the four occasions within a year starting in 2005.Movement from a rookery to a haulout was possible (due to our capture history structure) only between the third and fourth occasions in a year and from a haulout to a rookery between the fourth occasion in a year and the first occasion in the next year (Appendix 1).Including three separate daily surveys at rookeries prevented bias in estimates of female resighting and offspring detection probabilities that may have resulted from summarizing multiple observations when the number of observations per animal per occasion varied (Hastings et al., 2021).
We used a time-varying covariate for rookery occasions where "0" indicated "not seen before that year at a rookery" and "1" indicated "seen before that year at a rookery" (variable "sb", possible in the second and third rookery occasions, Appendix 1).This was included to allow female resighting probability to vary for the first versus subsequent resightings at a rookery within a year, which we suspected varied with reproductive state (e.g., females with no dependent may be more likely to be seen only once, and females with pup may be more likely to AIC were considered to be the most-supported models, particularly when ΔAIC was >3.0 (Burnham & Anderson, 2002).

| Nuisance parameters
covariance matrix equal to the negative Hessian of the log-likelihood function, following Johnson et al. (2016).
To correct the estimates of proportion with pup (B i ) for early pup mortality to 3 weeks of age (to provide an approximation of true birth probabilities, B i, corrected ), we fit three additional Cormack-Jolly-Seber models to the data from Hastings (2017) (2007( , Hastings, 2017) ) were used to correct estimates of B i using: B i, corrected = B i /φ pup 3 weeks, maternal age i .
We included the derived age-specific estimates of pup production (B i , the proportion of females alive that were with pups at the end of the pupping season) and survival in simple, deterministic Leslie matrix models using the R package popbio (Stubben & Milligan, 2007) to determine the effects of reproductive patterns on population trend estimates separately for the south region (Forrester and Hazy pooled), White Sisters and Graves Rocks.Population growth rate was estimated as the dominant eigenvalue of the Leslie matrix comprised of fully age-specific fecundity and survival schedules to age 30, assuming constant values after age 25, for an average year before the PMH and after the PMH.We calculated the 95% CI of estimated population trend using R and the delta method following Skalski et al. (2007) and Bowles et al. (2015).It was appropriate to use B i , the proportion of females alive that were with pups at the end of the pupping season which included early pup mortality, in these models because pups were marked at ~3 weeks of age and therefore first-year survival excluded early pup mortality.Therefore, these parameters provided complimentary survival and reproductive information for models.and 0.10 (both regions) were without a dependent.Important regional variation included earlier recruitment (age 4 rather than age 5) but thereafter slightly lower pup production and higher juvenile retention in the productive north region compared to the south (Figure 2).Important year variation included consistently lower pup production in both regions after the PMH (>2014; Figure 5), which if sustained in the south would result in population decline.We also found no evidence that reproductive state at the end of the pupping season affected female survival pre-or post-PMH.

| Reproductive performance and female survival
Concerning age and region effects on reproduction, females began pupping at younger ages in the north (age 4) than in the south (age 5; Figure 2a), which resulted in 0.14 and 0.30 more females With-Pup in the north than in the south at ages 4 and 5, respectively (Figure 2d).After the first age of recruitment for each region, the subsequent rate of recruitment was high and the same for both regions (0.515; Table 2).By age 8/9 (north/south), ~95% of females had recruited (Figure 2).In addition to regional differences in recruitment age, With-Pup females in the north were also more likely to have a dependent juvenile the year after producing a pup than their counterparts in the south (+0.09,With-Pup:With-Juvenile; Figure 3), which were more likely to have a pup in the year after producing a pup (With-Pup:With-Pup; Figure 3).2).With-juvenile females more often produced a pup the next year (0.483) than retained their juvenile for another year (0.328, Table 2).
The proportions of females with pup at the end of the pupping season (B i ) were higher in the north than in the south at age 4-5 due to earlier recruitment, but from age 6 until ages 18-20, B i in the north was ~0.05 lower than in the south (Figure 2a).Because (Figure 2).In a typical year pre-PMH at the end of the pupping season (including early pup mortality), ~0.60 to 0.65 of prime-aged females were with pup, ~0.25 to 0.30 were with juvenile, and ~0.10 had no dependent (Figure 2a, Table S1).Therefore, most parous females were with a dependent from year to year, until age 18-20 when transitioning to No-Dependent became more common (Figures 2 and 3).Senescence in birth probabilities was evident after age 12-13: by age 25, B i was ~0.40, J i was ~0.30, and N i was ~0.30, in both regions (Figure 2a).
By refitting data from Hastings (2017) to provide a simple correction to B i for early pup mortality, the model with a linear trend in pup survival with maternal age (ages 5-20) had the most support (AIC Weight = 0.46, vs. 0.20 and 0.17 for quadratic and spline fits, and 0.12 and 0.06 for two and three age categories, respectively).Early pup survival ranged from 0.76 for pups of age 5 mothers to 0.96 to pups of age 20 mothers (Figure 4).This correction was applied to estimates for both the north and south regions and produced estimates of true birth probabilities B i, corrected of 0.722 in the south and 0.664 in the north, at age 12, and shifted the peak reproductive ages slightly earlier (ages 10-12; Figure 2c).
Concerning year effects on reproduction, cohort variation in recruitment rates (five cohorts) was not supported, but year variation in the transition probability With-Pup:With-Juvenile was important (Figure 5, model 72, Appendix 4).Pup production (B i ) was high in 2014, and consistently lower after initial ocean warming in summer 2014 (Figure 5, Table S2).Compared to estimates <2014 (from a post hoc model with subsets of years pre-and post-PMH pooled, x north = 0.567, 95% CI: 0.496-0.631,females aged 12), the average B i among years was ~0.061 lower >2015 (x north = 0.506, 0.444-0.560),resulting in a greater proportion of prime-aged females with juveniles >2015, whereas proportion with no dependent did not change appreciably (Figure 5, Table S2).
Concerning female survival, age, region, and year effects on female survival are well documented (Hastings et al., 2023), and survival estimates in this study were consistent with past analyses of these data (Hastings et al., 2011(Hastings et al., , 2018(Hastings et al., , 2023, estimates provided in Table S3).In this paper we addressed female survival in relation to reproductive state at the end of the pupping season.No models that included the effect of reproductive state on female survival overall, by age-class, during poor survival years or after ocean warming in 2014 were supported (Appendix 4).
Concerning potential effects of reduced reproduction on population trend, when the resulting age-specific reproductive and survival probabilities were included in a Leslie matrix model using average pre-PMH values (pooled years <2011, Tables S1 and S3), estimated population growth rates were: r -south = −0.007(95% CI: −0.017, 0.002), r -White Sisters = 0.025 (0.014, 0.035), and r -Graves Rocks = 0.047 (0.031, 0.062).Reduced reproduction following the PMH was large enough to affect the estimates of population trend.
We replaced the B i values in the Leslie matrix with those for 2016 (because they were similar to average values >2014; see Figure 5).
If this lower average reproductive output is sustained, an r -south of −0.015 (−0.025, −0.006) would result, indicating a population decline in the south.

| Nuisance parameters: Female resighting probabilities, offspring detection probabilities, and female movement probabilities
For resighting probabilities of females at rookeries, probabilities were the lowest (x = 0.33-0.47)and similar for Adult Prebreeders 4+ and juvenile females aged 0-3 (Table 2, Appendix 4).Resighting probabilities of females With-Pup were also highest for smaller northern rookeries (e.g., +0.21 and + 0.10 for Graves Rocks-born and White Sisters-born, respectively, compared to southern-born females With-Pup, Table 2).At haulouts, annual variation in female resighting probabilities was high, where effort varied annually, compared to less annual variation in resighting probabilities at rookeries, where effort was also significant in the model but more consistent annually compared to haulouts (Figure 6).
At rookeries, resighting probabilities for With-Pup females were high (x = 0.54-0.73per day among rookeries) and did not vary for first versus subsequent resightings.Also at rookeries, the resighting probabilities for With-Juvenile females were much reduced for first (x = 0.07 per day) versus subsequent sightings (x = 0.46 per day) and this predictor had the greatest effect on ΔAIC for this parameter (Table 2, Appendix 4).Resighting probability was high for first sightings of No-Dependent females (x = 0.67, all rookeries were similar), but, unlike With-Juvenile females, was slightly lower (−0.19) for subsequent sightings.Juvenile females aged 0-3 and Adult Prebreeders 4+ had lower resighting probabilities at rookeries (x = 0.33-0.47among rookeries) but, similar to With-Juvenile females, resighting probability was higher on subsequent than first sightings (+0.14, Table 2).At haulouts, resighting probabilities were 0.24-0.30higher for No-Dependent and Prebreeder 4+ adult females compared to With-Juvenile females and juvenile females aged 0-3 (Figure 6b,c).
For offspring detection proabilities, only regional and reproductive state effects were fit: probabilities were higher for With-   2).

| DISCUSS ION
We estimated true birth probabilities at peak reproductive age 12 were 0.722 and 0.664 for females born in southern and northern Southeast Alaska, respectively.True birth probabilities may be higher than 0.664 at smaller and less dense northern rookeries, if neonatal survival is higher than at the large, dense Forrester Island rookery, which had particularly high early pup mortality (Hastings, 2017;Kaplan et al., 2008;Maniscalco et al., 2008) and was the source of our (pre-decline) and were 0.55 in 1985 and 1986 during a period of dramatic decline, due to high rates of late-term abortions for younger, lactating females (Pitcher & Calkins, 1981;Pitcher et al., 1998).Our estimates cannot be directly compared to these historical values without assuming similar population age structures, but the average birth probability for ages 6-15 in our study (0.630 and 0.683 for the north and south, respectively) was similar to pre-decline values.Alaska pre-PMH (Mathews et al., 2011;Pitcher et al., 2007), we found age-related demographic processes, particularly senescence, may be an important component of female reproductive strategies.
Reproductive senescence is expected for female mammals (Comizzoli & Ottinger, 2021) and a sharp drop in birth or pregnancy rates at older ages was observed in other otariid species (starting at ages 13-17; Dabin et al., 2004;Eberhardt, 1985;Hernández-Camacho et al., 2008;Melin et al., 2012).We observed a gradual drop in birth probabilities after the peak age (~−0.20 reduction from ages 12 to 21), most similar to that observed for Antarctic fur seals (Lunn et al., 1994), although the rate of decline in Steller sea lions after age 20 requires more study (n < 20 females seen per age after age 20; Appendix 2).
Reduced birth probabilities in older females were associated with increased retention of juveniles and also steep increases in the probability of being without any dependent (Figure 3), suggesting failure in reproductive physiology with age.Usually ~0.10 of females were without a dependent in a year; this proportion increased steeply after age 17-18 (to perhaps 0.30; Figure 2a).
The physiological mechanisms responsible for female reproductive aging (i.e., infertility) are very similar across vertebrate species, at the level of the whole organism, reproductive organs and germ cells, including: the depletion of egg reserves, loss of ovarian function, changes to the uterine environment, loss of cycles of reproductive hormones (especially circulating estradiol), decreased steroid production, and a decline in the estrogen-dependent endocrine and behavioral responses that drive reproduction (Ottinger, 2010).

Causal mechanisms underlying reproductive senescence in
Steller sea lions require study, but neonatal survival remained high for the oldest mothers (Figure 4), suggesting adequate maternal condition during the neonatal period for older females that produced pups (and/or the important role of maternal experience in early pup survival at the rookery).In an historical sample collected in 1975-1978 and 1985-1986, pregnancy rates were low for females aged 15+ compared to prime-aged females and all three of females aged 21-30 experienced reproductive failures for undetermined reasons (table 2 in Pitcher & Calkins, 1981;table 6 in Calkins & Goodwin, 1988).However, sample size of oldest females was very small (n = 13), which also may have precluded the ability to determine whether body condition declined for the oldest females in that sample (Pitcher et al., 1998).As commonly seen in otariids (Lunn et al., 1994;McKenzie et al., 2007;Melin et al., 2012), the recruitment rate (based on reproductive state at the end of pupping season) was high (0.515 per age) and recruitment occurred mainly over a few ages (ages 5-7; by young females resulted from recruitment and high neonatal mortality (Figure 4) and was associated with greater retention of their juveniles (Figure 3).High neonatal mortality of pups born to young mothers delayed the peak output of "viable" pups (pups that survived the period of high neonatal mortality at <3 weeks of age; Hastings, 2017) from ages 8-15 to ages 10-15 (Figure 2c).The probability of young mothers retaining a juvenile was up to 0.25 higher, but the probability of skipping pupping without a dependent juvenile was not appreciably higher than probabilities for prime-aged females (Figure 3).We suspect higher probability of retaining the juvenile results from higher abortion rates in younger lactating females, which are particularly affected by nutritional stress (Pitcher et al., 1998).More study is required to determine if this pattern is also associated with delayed weaning for offspring of young mothers, perhaps due to the smaller size and slower growth of their pups, which would allow them to reach a weaning size threshold important for future survival and reproduction, a key driver in population dynamics, the behavior of mothers and offspring, and reproductive strategies in Steller sea lions (Hastings et al., 2021).Reduced reproductive output of young female Steller sea lions is expected as asymptotic body mass is reached at later ages than recruitment (~age 13 in Steller sea lions: Winship et al., 2001), a common pattern in female pinnipeds (Boltnev & York, 2001;Dabin et al., 2004;Grandi et al., 2010;Laws, 1956), and probability of pregnancy during late gestation is strongly dependent on female mass and condition (Pitcher et al., 1998).
Regional variation in population dynamics suggests a favorable environment in northern Southeast Alaska, and larger body size of northern-born pups and smaller home ranges suggests animal density may be low relative to environmental productivity in the north (Hastings et al., 2011;Jemison et al., 2018;Mathews et al., 2011).
Formal studies of regional variation in sea lion prey abundance and composition in Southeast Alaska are lacking but high productivity in the north is suspected due to rapid and recent deglaciation in Glacier Bay resulting in new habitat (Mathews et al., 2011).This area is characterized by high levels of mixing, primary and secondary productivity, and dense forage fish schools which also concentrate in shallower depths during the day perhaps providing more efficient foraging for sea lions (reviewed by Rehberg et al., 2018).Areas of strong tidal currents also concentrate prey and serve as important corridors for migrating Pacific salmon; protections afforded by Glacier Bay National Park (including the Graves Rocks rookery) may also minimize threats and harassment to sea lions (reviewed by Rehberg et al., 2018).
A nutritional component for regional differences may be further supported by earlier recruitment of females at ages 4-5 in the north than in the south (Figure 2).Earlier recruitment in longlived mammals generally improves fitness, promotes population growth, and is indicative of high food abundance relative to animal density (Cole, 1954;Fowler, 1987;Stearns, 1976).However, after age 5, pup production averaged ~0.05 lower in the north than in the south, associated with a slightly greater retention of juveniles (Figure 3) likely due to higher offspring survival in the north than in the south (+0.11 and +0.07 from age 0-1 and 1-2, respectively, for northern-born offspring, Hastings et al., 2011).In fact, juvenile survival to age 4 was higher in northern Southeast Alaska than in all other areas studied from Oregon through Russia (Wright et al., 2017).Therefore, high population growth in the north (Mathews et al., 2011) may be driven by not only immigration (Jemison et al., 2013(Jemison et al., , 2018) ) and high juvenile survival (Hastings et al., 2011) but also younger ages of first reproduction rather than higher annual reproductive output.In addition, weaning ages were similar between regions within Southeast Alaska but sea lions in Southeast Alaska were smaller and weaned later than their counterparts west of Cook Inlet in the northern Gulf of Alaska, perhaps due to a less productive and/or more variable environment in which females may exist closer to the edge of their physiological capacity for producing successful offspring (Hastings et al., 2021).
This idea is supported by our observation that females produce offspring earlier but do not produce more offspring even in productive areas of Southeast Alaska, perhaps due to body-size and growth constraints and the need to commonly invest >1 year in offspring to ensure they are able to reach an appropriate size for successful weaning (Hastings et al., 2021, this study).
Surprisingly, a cost of reproduction on female survival was not detected in our study and causes for low adult female survival in 2014-2016 (Hastings et al., 2023) et al., 1998;Pitcher & Calkins, 1981;Pitcher et al., 1998).Also, during that decline, juvenile mortality was high, with potential periods of high adult mortality (Pendleton et al., 2006;York, 1994;York et al., 1996).We saw no evidence of a failure to properly buffer adult survival and offspring support or production during the PMH, similar to a study at Chiswell Island before the PMH (Maniscalco et al., 2014).However, reproductive status at the end of the pupping season may not sufficiently reflect survival costs and energy burdens over the next year: the energy balance of a female that loses her dependent shortly after the pupping season (due to death or weaning) may be similar to that of a female without a dependent at the end of the pupping season.Costs of reproduction may also be masked by effects of individual quality (Chambert et al., 2013;Hamel et al., 2009), suggesting that more study is needed to tease apart these potential confounding factors.
Although we found no evidence that low adult female survival in  (Bond et al., 2015;Chen et al., 2021;Danielson et al., 2022).Viable pup production was annually variable (up to ~0.20) and was particularly high in 2014 for unknown reasons (Figure 5).After 2014, the lower numbers of pups produced was associated with a greater probability of females retaining their juveniles but not an appreciably greater probability of females being without any dependent (Figure 5, Table S2).

ACK N OWLED G M ENTS
We especially thank Jeff Laake for statistical guidance during the initial phase of this study, and Ken Pitcher for initiating and expanding Codes for location: R = rookery, H = haulout, where only H was possible from 2001 to 2004 and on occasion 4 per year after 2004; R was possible only for occasion 1-3 per year after 2004.0 = female not seen.After 2004, survival was estimated and reproductive state transitions were possible only between occasion 4 in year x and occasion 1 in year x + 1. Reproductive surveys (conducted in late June-mid July) began in 2005 with three daily surveys per annual summer survey at the rookery (in yellow boxes) and one occasion at the haulout (summarizing any resighting at a haulout during the survey window that year, in gray boxes).A time-varying covariate, "seen before" (sb), was included for rookery occasions to allow female resighting probability to vary between the first and subsequent resightings within a year (see text, instances when females were seen on the previous rookery occasion are colored red).
be seen again after their first sighting).Six reproductive state transitions could be estimated: Prebreeder:With-Pup (from Prebreeder in year x to With-Pup in year x + 1), With-Pup:No-Dependent, With Pup:With-Juvenile, With-Juvenile:With-Pup, With-Juvenile:No-Dependent, and No-Dependent:With-Pup.The probability of remaining in the same state (Prebreeder:Prebreeder, With-Pup:With-Pup, With-Juvenile:With-Juvenile, No-Dependent:No-Dependent) was estimated as the difference of the other row-wise probabilities because multinomial variables must sum to 1 (Appendix 3).The probabilities of making impossible reproductive state transitions (shown in gray boxes in Appendix 3) were fixed to 0.We modeled parameters sequentially (beginning with the global or most complex model for all parameters and then simplifying): first nuisance parameters: female resighting probability, then offspring detection probability, then movement transitions, then parameters of biological interest: reproductive state transitions, and finally female survival probability in relation to reproductive state.Following the hypothesis testing framework ofLebreton et al. (1992), we modeled nuisance parameters first to improve precision of estimates and focus our analyses on our primary parameters of interest (and factors affecting them): reproductive state transitions and female survival probability.Models with fewer parameters and the lowest Our most important results (detailed below) included: important age variation in reproductive output was observed as a gradual increase in proportion of females with pup from the age of first recruitment to ~12 years of age, followed by gradual senescence to at least age 20 (Figure2).In a typical year before the PMH at peak reproductive ages, 0.60/0.65 of females (north/south) were with pup at the end of the pupping season, 0.30/0.25 were with juvenile, F I G U R E 2 Proportion of Steller sea lion females in Southeast Alaska (2005-2019) by reproductive state at the end of the pupping season by age and natal region.(a) Natal regions were South (Forrester and Hazy in open circles/dashed line) and North (White Sisters and Graves Rocks in solid circles and solid lines; Figure 1).(b) Estimates for natal region South with 95% CI.(c) Estimates of true birth probabilities: proportion of females With-Pup was corrected for early pup mortality from birth to age 3 weeks (see text).(d) Regional difference in the proportion of females with pup (North-South).PWP, Proportion With-Pup.Estimates shown are for years <2011.
In addition to recruitment probability, age effects were important predictors of transitions from With-Pup.With-Pup:With-Pup was highest at middle ages, and With-Pup:With-Juvenile and With-Pup:No-Dependent were the highest for the oldest females (especially in With-Pup:No-Dependent after age 18-20) and the youngest females (Figure 3).Transitions from With-Juvenile and No-Dependent did not vary with age or region (Table 2, Appendix 4).Although model selection suggested some age variation in the transition probability No-Dependent:With-Pup, estimates of 0 and 1 (i.e., at the parameter-space boundary and possibly unreliable) were produced (perhaps due to small numbers of No-Dependent females; Figure 2a).Therefore, we modeled this parameter as constant with age.Probabilities of transitioning to No-Dependent were low (No-Dependent:No-Dependent = 0.143; With-Juvenile:No-Dependent = 0.188, and With-Pup:No-Dependent ~0.05 until age 18-20; Figure 3, Table of recruitment and higher transition probabilities With-Pup:With-Juvenile and With-Pup:No-Dependent for younger mothers (Figure 3), females did not reach peak pup production age until 12-13 the lowest for females born at the large southern rookeries (Forrester = 0.34, 0.31-0.37,Hazy = 0.39, 0.35-0.44,White Sisters and Graves Rocks pooled: 0.48, 0.44-0.53).For movement parameters, the global model could not be simplified (Appendix 4).Resulting movement estimates were reasonable: juvenile females 0-3 used rookeries less than other groups, and juvenile females aged 0-3 and With-Juvenile adult females moved between rookeries and haulouts more than other groups in the same survey year (Table

F
I G U R E 3 Probability of transitioning reproductive states for Steller sea lion females With-Pup in Southeast Alaska by age and natal region.Natal regions were South (Forrester and Hazy in open circles/dashed line) and North (White Sisters and Graves Rocks in solid circles and solid lines; Figure 1).Estimates plotted are for the years <2011.F I G U R E 4 Survival of Steller sea lion pups to 3 weeks of age based on maternal age at Forrester Islands, Southeast Alaska, from 2007 to 2014.Models were refit to the data from Hastings (2017) to also include models that estimated effect of maternal age on pup survival as a continuous variable (see text).Estimates for an average/good year (2007) are shown.Blue ribbon is 95% CI. neonatal mortality correction estimate.These estimates are similar to the 0.70 estimate for branded Forrester females in 2004 at ages 9-10 (Taylor & Boor, 2012) and for females of all ages at Chiswell Island, Alaska from 2003 to 2012(Maniscalco et al., 2014).If a similar pattern occurs with age for Chiswell Island females, birth probabilities at peak ages would be higher at that rookery than in Southeast Alaska.A recent estimate for Steller sea lion females in the northern Gulf of Alaska also suggests higher peak reproductive output in this area (0.80,Warlick et al., 2022).Birth probability estimates for females in the Gulf of Alaska based on cross-sectional data were 0.63 during[1975][1976][1977][1978] Our estimates of peak reproductive output in Steller sea lions in Southeast Alaska were moderately high compared to those for other otariids.Our estimates were similar to published estimates for subantarctic fur seals, Arctocephalus tropicalis, on Amsterdam Island (0.721 at age 12;Dabin et al., 2004) and New Zealand fur seals, Arctocephalus forsteri, at Kangaroo Island (0.60-0.70 at age 8+;McKenzieet al., 2007), and much higher than the endangered Galapagos sea lion, Zalophus wollebaeki (0.40-0.48 at ages 6+;Kalberer et al., 2018).In contrast, our estimates at peak ages were lower than published estimates for the California sea lion, Zalophus californianus (0.77-0.80;Hernández-Camacho et al., 2008;Melin et al., 2012), the endangered New Zealand Sea Lion, Phocarctos hookeri (~0.75 to 0.88 at age 7+;Childerhouse et al., 2010) and the Antarctic fur seal, Arctocephalus gazella (0.80 at ages 7-9 at Bird Island;Lunn et al., 1994;    0.90 at ages 8-16 at Livingston Island;Schwarz et al., 2013).Although the combined survival probabilities and reproductive output was sufficient for population stability or growth in Southeast F I G U R E 5 Annual variation in the proportion of female Steller sea lions (a) With-Pup or (b) With-Juvenile in Southeast Alaska, 2005-2019.Blue ribbons are 95% CI.Estimates plotted are for females aged 12 (peak pupping age, see Figure 2a) born in the North (White Sisters or Graves Rocks; Figure 1).
However, parturition dates were later for the oldest mothers (parturition dates became earlier from ages 5 to 12 and then became later from ages 12 to 20; Hastings & Jemison, 2016; but see Maniscalco & Parker, 2018) and later parturition dates were associated with poor body condition in other species (reviewed by Hastings & Jemison, 2016).

Figure
Figure 2a).This figure is likely an underestimate of recruitment rate based on all live births, because our recruitment rate estimates were based on pup production at the end of the pupping season and early pup mortality is higher in younger than older mothers (Fig-ure 4).Compared to prime-aged females, reduced pup production may have similarly impacted females with and without dependents.If negative changes to the prey field during the PMH (Suryan et al., 2021) contributed to adult female mortality, we expected that females with dependents would be especially impacted.If our result is correct, it suggests female Steller sea lions are physiologically fine-tuned to their environment: during a period of steep population decline from 1975 to 1986, lactating females aborted their fetuses during mid-tolate gestation (essentially all mature females were pregnant and implanted annually by late fall), reducing birth rates by 0.08 and this was accompanied by smaller body size of females (Calkins 2014-2016 was related to reproductive state at the end of the pupping season, pup production remained consistently at lower levels (−0.06 from the mean from 2005 to 2013) in Southeast Alaska following ocean warming in 2014 (from 2015 to 2019; Figure 5).Warm surface water reached the coast of Southeast Alaska in springsummer of 2014 with peak temperatures in 2015-2016, cooled in 2017 and warmed again in spring 2019 reproductive surveys in Alaska.This work was made possible by the many individuals who marked and resighted Steller sea lions in Alaska over several decades, especially T. Gage, S. Goodglick, J. Jenniges, C. Kaplan, J. King, S. Lewis, D. McCallister, K. Raum-Suryan, L. Rea, M. Rehberg, G. Snedgen, B. Van Burgh, J. Westlund, and dedicated Lowrie Island field crews.We are grateful for resighting data provided by the members of the public and collaborating agencies, including Glacier Bay National Park, Alaska SeaLife Center, and the Marine Mammal Laboratory.We are grateful to anonymous reviewers for suggestions which improved this manuscript.This research was conducted under permits issued by the NMFS to the ADFG (US Marine Mammal Permits 358-1564, 358-1888, 14325, 18537, and 22298), with additional permits granted by the US National Park Service, the US Fish and Wildlife Service-Alaska Maritime National Wildlife Refuge, and the Department of Fisheries and Oceans Canada.Funding was provided by the NMFS, Alaska Region, through awards: NA17FX1079, NA04NMF4390170, NA08NMF4390544, NA11NMF4390200, NA15NMF4390170, NA16NMF4390029, NA19NMF4390084, and NA21NMF4720035 to the ADFG.Funding was also provided by the State of Alaska.The findings and conclusions in this paper are those of the author(s) and do not necessarily represent the views of the NMFS.Example capture histories for Steller sea lion females in Southeast Alaska.Codes for reproductive state: B = With-Pup, J = With-Juvenile, u = uncertain, P = Prebreeder (only possible on the first release).

parameters: Proportions of females alive by reproductive state, corrections for early pup mortality, and resulting estimates of population trend
aged 4+ or No-Dependent females, and (8) With-Pup or With-Juvenile females.Natal rookery effects were fit only for groups at rookeries.We fit 17 additional models.For offspring detection probability, our global model included separate estimates for With-Pup and With-Juvenile at each natal rookery group (nr2) [nr2:B + nr2:J] where nr2 was Forrester, Hazy, and White Sisters/ Graves Rocks pooled (Figure 1); we fit four additional models.For movement transitions between haulouts (H) and rookeries (R), our global model was [HtoR:togroup year x + 1 + RtoH:group year x ], where group was five groups (Juveniles aged 0-3/Adult Prebreeders 4+/ With-Pup/With-Juvenile/No-Dependent); we fit three simpler models by simplifying group.Models for movement transition parameters were influenced by observed patterns.Only one marked female was observed with a pup at a haulout (W330 at South Marble Island in 2010); few pups were produced at haulouts in Southeast Alaska (from 2010 to 2019: average of 0.6% of pups were at haulouts during aerial surveys, or 39 at haulouts vs. 6504 at rookeries; Alaska Fisheries Science Center, 2023).Only three females were observed with pup at a rookery and also seen at a nearby haulout in the same survey year (Graves Rocks and Inian Islands: ~30 km distant, Hazy Island and Sea Lion Rocks Puffin Bay: ~45 km, and Lowrie Island and Wolf Rock: ~20 km; For reproductive state transitions, our global model was [Recruit:old + Recruit:new:region:age 3/4/5p + With-Pup:With-Juvenile + With-Pup:No-Dependent + With-Juvenile:With-Pup + With-Juvenile:No-Dependent + No-Dependent:With-Pup], where region was natal region (north/south; Figure 1), old was the 1994-1995 cohorts and els in which survival was affected by reproductive state, by reproductive state*age or *year (the three poor years of survival 2014-2016 and 2014+, the years during and following the PMH).2.3 | DerivedDerived parameters calculated as functions of estimated reproductive state transitions from the best model included the proportion of the female population alive at each age i that were of reproductive states Prebreeder (P i ), With-Pup (B i ), With-Juvenile (J i ), and No-Dependent(N i ).Givenfemale survival probabilities did not vary with reproductive state (see Results 3), estimates of these proportions for the first age possible for each reproductive state were calculated following equations: P 1st age = 1 − ̂ P:B−1st age , B 1st age = ̂ P:B−1st age , J 1st age = ̂ B:J−1st age , N 1st age = ̂ B:N−1st age .Proportions for subsequent ages i were calculated following equations:where ̂ was the estimated probability of changing reproductive states between years (e.g., ̂ P:B,i − 1 to i was the estimated probability of transitioning from Prebreeder at age i − 1 to With-Pup at age i or Prebreeder:With-Pup). Confidence intervals (95% CI) for derived values were approximated using a multivariate normal parametric bootstrap with the mean equal to the maximum likelihood estimate and the Estimates of female resighting probabilities per day at rookeries (estimates for 2008 are shown) and the probabilities of transitioning between reproductive states and moving between rookeries (R) and haulouts (H) for female Steller sea lions in Southeast Alaska,2005-2019.
Estimation of six possible reproductive state transitions used to examine age-specific reproductive performance of female Steller sea lions in Southeast Alaska, 2005-2019.The probability of remaining in the same state was estimated as the difference of the other row-wise probabilities which, as multinomial variables, must sum to 1 (in red in yellow boxes).Impossible reproductive state transitions (in gray boxes) were fixed to 0. Four possible reproductive states were: P = Prebreeder (nulliparous), With-Pup, With-Juvenile, and No-Dependent (parous).